Original ArticlesManaging for change: Using vertebrate at sea habitat use to direct management efforts
Introduction
Recent changes to the Earth’s climate are well documented, unequivocal and are effecting a wide range of species and communities from the equator to the poles in both terrestrial and marine ecosystems (e.g. Parmesan, 2006). Polar regions are experiencing some of the strongest and fastest large-scale physical changes anywhere on Earth, with rapid rises in atmospheric and oceanic temperatures (Meredith and King, 2005, Chapman and Walsh, 2007) and accelerating loss of ice sheet mass (Pritchard et al., 2012). In the Southern Ocean, there is increasing evidence of the impacts of such changes on biological systems at various trophic levels (e.g. McMahon and Burton, 2005, Montes-Hugo et al., 2009, Flores et al., 2012, Ropert-Coudert et al., 2015). Despite this, the links between physical changes and biological productivity remain poorly understood. However, any biological effects will ultimately be reflected in the responses of higher-trophic level species (seals, seabirds and whales) because they integrate and amplify the effects occurring at lower trophic levels (Hindell et al., 2003, Costa et al., 2010), often making them useful indicators of wider ecosystem change.
A change in distribution is one potential response to climate change (Walther et al., 2002, Mueter and Litzow, 2008, Trathan and Agnew, 2010) as species are forced towards higher latitudes or altitudes. Recently, studies into the distribution of highly mobile marine predators have focussed on predicting species responses to future climate change (e.g. Péron et al., 2012, Hazen et al., 2013, Spencer et al., 2016). However, to properly understand current and future distributions it is essential to establish historical distributions as baselines against which changes can be assessed (Lotze and Worm, 2009). Historical records are often brief or fragmented (Swetnam et al., 1999) and biased towards terrestrial ecosystems (Elith and Leathwick, 2009). For marine environments, historical distributions are mostly available for species of commercial interest (Bellier et al., 2007, Nye et al., 2009) and typically do not exist for remote regions such as the Southern Ocean. Conversely, baseline environmental data from remotely sensed sources (satellite) have been available since the 1980’s, before the widespread use of animal-tracking devices to observe habitat use and at-sea distributions. Environmental data can be used to construct habitat models or Species Distribution Models (SDMs), which correlate species occurrence with environmental variables to explain or predict a species’ distribution (Robinson et al., 2011). The inclusion of historical environmental data has the potential to hindcast SDMs to the likely historical distribution of top predators (Louzao et al., 2013), providing a baseline to assess future change and inform and appraise management decisions.
As well as potential changes over decadal time scales, the spatial distribution of many pelagic predators can be highly variable over shorter periods, such as inter-annually or seasonally (Forney and Barlow, 1998, Pettex et al., 2012). This temporal variability is a major source of uncertainty in marine resource management and the effectiveness of SDMs as a management tool is determined in part by their ability to capture year-round habitat conditions (Becker et al., 2014). For species known to have pronounced seasonality in distribution, as is the case for many Southern Ocean predators (Cockell et al., 1999), SDMs that are spatio-temporally explicit at scales relevant to species movements and management objectives, will likely prove more informative. Although SDMs are under-utilised in marine species (Robinson et al., 2011) they have been effectively employed to inform habitat conservation, understand fisheries interactions and investigate the impacts of climate change in pelagic predators (See Robinson et al., 2011). Yet often, many do not consider the temporal shifts in habitat use and spatial distribution that can occur in wide-ranging animals.
In highly variable environments such as the Southern Ocean, significant environmental changes including the growth and decay of sea ice, seasonal movement of fronts, and fluctuations in primary productivity can occur on relatively short time scales of weeks to months (Gordon, 1981, Clarke, 1988, Sokolov and Rintoul, 2009). Such rapid environmental change can alter prey availability and the distribution of foraging predators (Cockell et al., 1999). Therefore, incorporation of temporal variability into SDMs for Southern Ocean predators is important for a variety of management approaches such as the design of marine protected areas, quantification of potential fisheries interactions and development of accurate ecosystem models.
Within this context, we studied the winter distribution of female Antarctic fur seals (Arctocephalus gazella, Peters, 1875), a highly mobile pelagic predator, from three Southern Ocean populations. In the context of the current biogeography of the species, following recovery after massive exploitation in the 18th and 19th centuries (Payne, 1977) and by expanding SDMs previously established for each population (Arthur et al., 2017) this study aims to: (1) Establish likely historical fur seal foraging habitat as a baseline to assess whether habitat quality has changed over recent decades, (2) describe temporal variability in foraging habitats across the non-breeding period and (3) assess the degree of spatio-temporal overlap with Southern Ocean management areas and the potential for interaction with fisheries during winter.
Section snippets
Tracking instrumentation and analysis
Female Antarctic fur seals were tracked during their non-breeding winter migrations (April–December) at three colonies: Marion Island (Prince Edward Islands, 2008–13), Bird Island (South Georgia, 2008–11) and Cape Shirreff (South Shetland Islands, 2008–10) (Fig. 1a). Seals were equipped with a global-location sensing logger (GLS; British Antarctic Survey, Cambridge UK, 2.5–3.6 g) towards the end of lactation that was recovered when animals returned to pup the following season (n = 184). Animal
Environmental change and retrospective habitat modelling
There were clear long-term trends in several environmental parameters across the spatial domain of our study over recent decades, most notably SST, WIND and ICE (Fig. 2, Supporting Information Fig. A1). Around Marion Island, there was an overall warming trend of SST (r > 0.2) and decrease in WIND (r < −0.2) across contemporary core fur seal habitats, while ICE showed an increasing trend in the southern core habitats. Sea surface temperature also had a warming trend in contemporary core areas
Baseline foraging habitats of antarctic fur seals
By hindcasting pre-existing SDMs we have provided estimates of the historical foraging habitats for three Antarctic fur seal populations in the Southern Ocean. This necessitated extrapolating in environmental space, which is inherently risky as, in this instance, there are no past observations to support predictions (Elith and Leathwick, 2009). However, such extrapolation is necessary if we are to explore how currently used winter habitats might have changed over the past 25 years, a vital step
Author contributions
BA, MAL, MH, PT and MG conceived the ideas and designed the study. BA, MB, NDB undertook fieldwork and data collection. BA, MH and MAL analysed the data. BA, MAL, MH and MG wrote the paper. All authors contributed critically to the drafts and gave final approval for publication.
Acknowledgements
We are grateful to the many field teams at Marion Island (2008–13), Bird Island (2008–11) and Cape Shirreff (2008–10) who have deployed and recovered tags. We acknowledge the logistical support provided by the South African National Antarctic Program (SANAP), the British Antarctic Survey (BAS) and the U.S. Antarctic Marine Living Resources (US AMLR) Program. Thank you to Mike Sumner and Ben Raymond for providing analytical support and to Keith Reid for his advice during analysis and manuscript
References (98)
- et al.
Winter habitat predictions of a key Southern Ocean predator, the Antarctic fur seal (Arctocephalus gazella)
Deep Sea Res. Part II
(2017) Seasonality in the Antarctic marine environment
Compar. Biochem. Physiol. Part B
(1988)- et al.
Historical baselines for large marine animals
Trends Ecol. Evol.
(2009) - et al.
Sea ice in the western Antarctic Peninsula region: Spatio-temporal variability from ecological and climate change perspectives
Deep Sea Res. Part II
(2008) - et al.
The South Georgia and the South Sandwich Islands MPA: protecting a biodiverse oceanic island chain situated in the flow of the Antarctic Circumpolar Current
Adv. Mar. Biol.
(2014) - AFMA, 2003. Antarctic Fisheries Bycatch Action Plan. Australian Fisheries Management Authority....
Review – The CCAMLR ecosystem monitoring programme
Antarctic Sci.
(1997)- et al.
Sea ice: a critical habitat for polar marine mammals and birds
- et al.
Return customers: foraging site fidelity and the effect of environmental variability in wide-ranging antarctic fur seals
PLoS One
(2015) - et al.
South for the winter? within-dive foraging effort reveals the trade-offs between divergent foraging strategies in a free-ranging predator
Funct. Ecol.
(2016)
Oceanic circumpolar habitats of Antarctic krill
Mar. Ecol. Progr. Series
Pup weight and survival of northern fur seals Callorhinus ursinus
J. Zool.
Predicting seasonal density patterns of California cetaceans based on habitat models
Endangered Spec. Res.
Ecology: From Individuals to Ecosystems
Historical fluctuations in spawning location of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) in the Bay of Biscay during 1967–73 and 2000–2004
Fish. Oceanogr.
Pup production and distribution of breeding Antarctic fur seals (Arctocephalus gazella) at South Georgia
Antarctic Sci.
Individual variation in the duration of pregnancy and birth date in Antarctic fur seals: the role of environment, age, and sex of fetus
J. Mammal.
Population demography of Antarctic fur seals: the costs of reproduction and implications for life-histories
J. Anim. Ecol.
Dispersal of male and female Antarctic fur seals (Arctocephalus gazella)
Canad. J. Fish. Aquat. Sci.
Report of the Twenty-Eighth Meeting of the Commission
CCAMLR Statistical Bulletin 27
A synthesis of Antarctic temperatures
J. Clim.
Overwintering strategies of Antarctic organisms
Environ. Rev.
Approaches to studying climatic change and its role on the habitat selection of Antarctic pinnipeds
Integr. Compar. Biol.
Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976–1987: implications for Southern Ocean monitoring studies
Diet, provisioning and productivity responses of marine predators to differences in availability of Antarctic krill
Mar. Ecol. Progr. Series
Management of Southern Ocean fisheries: global forces and future sustainability
Antarctic Sci.
Bathymetry and frontal system interactions influence seasonal foraging movements of lactating subantarctic fur seals from Marion Island
Mar. Ecol. Progr. Series
Proposal for a conservation measure establishing an East Antarctic Representative System of Marine Protected Areas – CCAMLR-XXXII/34 Rev.1
Report of the Thirty-second Meeting of the Commission
Proposal for a Representative System of Marine Protected Areas (RSMPA) in the East Antarctica planning domain – SC-CAMLR-XXX/11
Report of the Thirteenth Meeting of the Scientific Committee
A proposal for the establishment of a Ross Sea Region Marine Protected Area – CCAMLR-XXXII/27
Report of the Thirty-second Meeting of the Commission
Species distribution models: Ecological explanation and prediction across space and time
Ann. Rev. Ecol. Evol. System.
Impact of climate change on Antarctic krill
Mar. Ecol. Progr. Series
Climate change selects for heterozygosity in a declining fur seal population
Nature
Life history buffering in Antarctic mammals and birds against changing patterns of climate and environmental variation
Global Change Biol.
Seasonal patterns in the abundance and distribution of California cetaceans, 1991–1992
Mar. Mammal Sci.
Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer
J. Anim. Ecol.
Seasonality of Southern Ocean sea ice
J. Geophys. Res. Oceans
Spatial distribution of foraging in female Antarctic fur seals Arctocephalus gazella in relation to oceanographic variables: a scale-dependent approach using geographic information systems
Mar. Ecol. Progr. Series
Making marine protected areas work
Nature
Predicted habitat shifts of Pacific top predators in a changing climate
Nat. Clim. Change
Ecosystem monitoring: are seals a potential tool for monitoring change in marine systems?
Dynamic ocean management: integrating scientific and technological capacity with law, policy, and management
Stanford Environ. Law J.
Population changes in Subantarctic and Antarctic fur seals at Marion Island
South Afr. J. Wildlife Res.
Seal mitigation measures on trawl vessels fishing for krill in CCAMLR Subarea 48.3
CCAMLR Sci.
Cited by (12)
Southern Ocean isoscapes derived from a wide-ranging circumpolar marine predator, the Antarctic fur seal
2020, Ecological IndicatorsCitation Excerpt :This enables monitoring of year-round habitat use, of specific value in designing effective conservation planning and ecosystem management strategies. For example, the retrospective-isotope analysis approach could be particularly useful in identifying regions that may currently fall outside of areas of active management (e.g. CCAMLR/CEMP management areas, marine protected areas, Arthur et al., 2018). Foraging location explained significant variation in seal δ13C values during the 8-month inter-breeding period.
Extrapolation in species distribution modelling. Application to Southern Ocean marine species
2020, Progress in OceanographyCitation Excerpt :SDM is also used to define species distribution spatial range (Nori et al. 2011, Walsh and Hudiburg 2018) and can be used as decision criteria for conservation purposes (Guisan et al. 2013, Marshall et al. 2014). For instance, it is currently used in proposals developed by national committees of the CCAMLR (Commission for the Conservation of Antarctic Marine Living Resources) to support the definition and delineation of marine protected areas (Ballard et al. 2012, CCAMLR report WG-FSA-15/64, Arthur et al. 2018). Applying SDM to Southern Ocean case studies is particularly challenging due to major constraints and biases that may reduce modelling performance.
No evidence of microplastics in Antarctic fur seal scats from a hotspot of human activity in Western Antarctica
2020, Science of the Total EnvironmentCitation Excerpt :Further research that directly looks for microplastics in the guts of krill, myctophid fishes, and dead stranded fur seals would provide further insights into the prevalence of microplastic pollution in the pelagic ecosystem of the Bransfield Strait and elsewhere off Antarctica. Another relevant point is the northward migration of female fur seals during winter (Arthur et al., 2018), which leads them to areas with higher levels of microplastic pollution (Perez-Venegas et al., 2018). Information are scarce about the winter habitat of male fur seals breeding in the South Shetland Islands, but they would presumably be less exposed than females to microplastic pollution if they remained south of the Antarctic Polar Front year-round.
Spatial and temporal diving behavior of non-breeding common murres during two summers of contrasting ocean conditions
2019, Journal of Experimental Marine Biology and EcologyCitation Excerpt :For example, predators may exhibit site specialization despite environmental gradients (Patrick et al., 2014). Alternatively, marine predators may dynamically adjust their foraging locations and diving patterns as conditions change (Abecassis et al., 2013; Kowalczyk et al., 2015; Arthur et al., 2018). Therefore, assessing localized foraging areas for predators during years with varying conditions is essential for understanding flexibility across individuals in foraging behavior.
Efficacy of species distribution models (SDMs) for ecological realms to ascertain biological conservation and practices
2023, Biodiversity and ConservationMarine mammal consumption and fisheries removals in the Nordic and Barents Seas
2022, ICES Journal of Marine Science